Abstract
Sustained changes in mood or action require persistent changes in neural activity, but it has been difficult to identify the neural circuit mechanisms that underlie persistent activity and contribute to long-lasting changes in behavior. Here, we show that a subset of Doublesex+ pC1 neurons in the Drosophila female brain, called pC1d/e, can drive minutes-long changes in female behavior in the presence of males. Using automated reconstruction of a volume electron microscopic (EM) image of the female brain, we map all inputs and outputs to both pC1d and pC1e. This reveals strong recurrent connectivity between, in particular, pC1d/e neurons and a specific subset of Fruitless+ neurons called aIPg. We additionally find that pC1d/e activation drives long-lasting persistent neural activity in brain areas and cells overlapping with the pC1d/e neural network, including both Doublesex+ and Fruitless+ neurons. Our work thus links minutes-long persistent changes in behavior with persistent neural activity and recurrent circuit architecture in the female brain.
Highlights
Social behaviors are known to be affected by persistent internal states (Anderson, 2016; Berridge, 2004; Lorenz and Leyhausen, 1973)
To investigate the neural basis of a persistent internal state in the female brain, we focused on pC1 neurons, one of eight Doublesex-expressing cell types in the central brain (Figure 1A; Kimura et al, 2015)
We found that activation of pC1-Int neurons induces a persistent effect on female receptivity and responses to male song, but that this effect diminishes with a delay period between neural activation and introduction of a male. pC1-Int-activated females copulated significantly faster than controls in the d0 condition, with reduced copulations following a delay between optogenetic activation and introduction of a male (Figure 1F)
Summary
Social behaviors are known to be affected by persistent internal states (Anderson, 2016; Berridge, 2004; Lorenz and Leyhausen, 1973). Activation of pC1 neurons affects receptivity toward males (Wang et al, 2020b; Zhou et al, 2014), drives chasing of males (Rezaval et al, 2016; Wu et al, 2019), and aggressive behaviors toward females (PalavicinoMaggio et al, 2019; Schretter et al, 2020) These data suggest that female pC1 neurons can drive an arousal state, similar to male P1 neurons, but whether female pC1 neurons can drive persistent changes in behavior and persistent neural activity, has not yet been investigated. Direct measurements of synaptic connectivity can determine whether recurrent neural networks, known to be important for persistent neural activity lasting for seconds (Aksay et al, 2007), underlie minutes-long persistent activity and changes in behavior, as has been recently proposed for male mice and flies (Jung et al, 2020; Kennedy et al, 2020). We link minutes-long persistent neural activity and behavior with reciprocal connectivity in the female brain
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